Glycinebetaine protects plants against abiotic stress: Mechanisms and biotechnological applications

Plant, Cell and Environment

Volumn 34, Issue 1, 2011, Pages 1-20

  Chen, Tony H H ^a   Murata, Norio ^b  

^a OREGON STATE UNIVERSITY   (United States)

^b NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

Abiotic stress tolerance; Antioxidative defence; Glycinebetaine; Photoinhibition; Reactive oxygen species

Indexed keywords

BETAINE; REACTIVE OXYGEN METABOLITE;

ANTIOXIDANT; BIOACCUMULATION; BIOTECHNOLOGY; CELL ORGANELLE; DEVELOPMENTAL BIOLOGY; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; FLOWER; FRUIT; GENE EXPRESSION; GENETICALLY MODIFIED ORGANISM; LIFE CYCLE; OSMOSIS; OXYGEN; PHOTOINHIBITION; SOLUTE; TOLERANCE; TRANSGENIC PLANT;

ADAPTATION; ARTICLE; BACTERIAL GENE; BIOTECHNOLOGY; CHEMISTRY; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETICS; METABOLISM; METHODOLOGY; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT; PLANT GENE; REPRODUCTION; TRANSGENE; TRANSGENIC PLANT;

ADAPTATION, PHYSIOLOGICAL; BETAINE; BIOTECHNOLOGY; GENE EXPRESSION REGULATION, PLANT; GENES, BACTERIAL; GENES, PLANT; GENETIC ENGINEERING; PHOTOSYNTHESIS; PLANTS; PLANTS, GENETICALLY MODIFIED; REACTIVE OXYGEN SPECIES; REPRODUCTION; STRESS, PHYSIOLOGICAL; TRANSGENES;

EID: 78650024226     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2010.02232.x     Document Type: Article

References (129)

1. Ahmad R., Kim M.D., Back K.H., Kim H.S., Lee H.S., Kwon S.Y., Murata N., Chung W.I. & Kwak S.S. (2008) Stress-induced expression of choline oxidase in potato plant chloroplasts confers enhanced tolerance to oxidative, salt, and drought stresses. Plant Cell Reports 27, 687-698.
2. Alia, Hayashi H., Chen T.H.H. & Murata N. (1998a) Transformation with a gene for choline oxidase enhances the cold tolerance of Arabidopsis during germination and early growth. Plant, Cell & Environment 21, 232-239.
3. Alia, Hayashi H., Sakamoto A. & Murata N. (1998b) Enhancement of the tolerance of Arabidopsis to high temperatures by genetic engineering of the synthesis of glycinebetaine. The Plant Journal 16, 155-161.
4. Alia, Sakamoto A., Nonaka H., Hayashi H., Saradhi P.P., Chen T.H.H. & Murata N. (1999) Enhanced tolerance to light stress of transgenic Arabidopsis plants that express the codA gene for a bacterial choline oxidase. Plant Molecular Biology 40, 279-288.
5. Allakhverdiev S.I. & Murata N. (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochimica et Biophysica Acta 1657, 23-32.
6. Allakhverdiev S.I., Nishiyama Y., Miyairi S., Yamamoto H., Inagaki N., Kanesaki Y. & Murata N. (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiology 130, 1443-1453.
7. Allakhverdiev S.I., Los D.A., Mohanty P., Nishiyama Y. & Murata N. (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochimica et Biophysica Acta 1767, 1363-1371.
8. Allard F., Houde M., Krol M., Ivanov A., Huner N.P.A. & Sarhan F. (1998) Betaine improves freezing tolerance in wheat. Plant & Cell Physiology 39, 1194-1202.
9. Al-Taweel K., Iwaki T., Yabuta Y., Shigeoka S., Murata N. & Wadano A. (2007) A bacterial transgene for catalase protects translation of D1 protein during exposure of salt-stressed tobacco leaves to strong light. Plant Physiology 145, 258-265.
10. Aro E.M., Virgin I. & Andersson B. (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochimica et Biophysica Acta 1143, 113-134.
11. Asada K. (1999) The water-water cycle in chloroplasts: scavenging of active oxygen species and dissipation of excess photons. Annual Review of Plant Physiology & Plant Molecular Biology 50, 601-639.
12. Ashraf M. (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnology Advances 27, 84-93.
13. Bhatnagar-Mathur P., Vadez V. & Sharma K.K. (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Reports 27, 411-424.
14. Bhuiyan N.H., Hamada A., Yamada N., Rai V., Hibino T. & Takabe T. (2007) Regulation of betaine synthesis by precursor supply and choline monooxygenase expression in Amaranthus tricolor. Journal of Experimental Botany 58, 4203-4212.
15. Breitkreuz K.E., Shelp B.J., Fischer W.N., Schwacke R. & Rentsch D. (1999) Identification and characterization of GABA, proline and quaternary ammonium compound transporters from Arabidopsis thaliana. FEBS Letters 450, 280-284.
16. Chen S., Gollop N. & Heuer B. (2009) Proteomic analysis of salt-stressed tomato (Solanum lycopersicum) seedlings: effect of genotype and exogenous application of glycinebetaine. Journal of Experimental Botany 60, 2005-2019.
17. Chen T.H.H. & Murata N. (2002) Enhancement of tolerance to abiotic stress by metabolic engineering of betaines and other compatible solutes. Current Opinion in Plant Biology 5, 250-257.
18. Chen T.H.H. & Murata N. (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends in Plant Science 13, 499-505.
19. Cuin Y.A. & Shabala S. (2007) Compatible solutes reduce ROS-induced potassium efflux in Arabidopsis roots. Plant, Cell & Environment 30, 875-885.
20. Deshnium P., Los D.A., Hayashi H., Mustardy L. & Murata N. (1995) Transformation of Synechococcus with a gene for choline oxidase enhances tolerance to salt stress. Plant Molecular Biology 29, 897-907.
21. Desingh R. & Kanagaraj G. (2007) Influence of salinity stress on photosynthesis and antioxidative systems in two cotton varieties. General & Applied Plant Physiology 33, 221-234.
22. Einset J. & Connolly E.L. (2009) Glycine betaine enhances extracellular processes blocking ROS signaling during stress. Plant Signaling & Behavior 4, 197-199.
23. Einset J., Nielsen E., Connolly E.L., Bones A., Sparstad T., Winge P. & Zhu J.K. (2007) Membrane-trafficking RabA4c involved in the effect of glycine betaine on recovery from chilling stress in Arabidopsis. Physiologia Plantarum 130, 511-518.
24. Einset J., Winge P., Bones A.M. & Connolly E.L. (2008) The FRO2 ferric reductase is required for glycine betaine's effect on chilling tolerance in Arabidopsis roots. Physiologia Plantarum 134, 334-341.
25. Flexas J. & Medrano H. (2002) Drought inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Annals of Botany 89, 183-189.
26. Fujiwara T., Hori K., Ozaki K., Yokota Y., Mitsuya S., Ichiyanagi T., Hattori T. & Takabe T. (2008) Enzymatic characterization of peroxisomal and cytosolic betaine aldehyde dehydrogenase in barley. Physiologia Plantarum 134, 22-30.
27. Gao M., Sakamoto A., Miura K., Murata N., Sugiura A. & Tao R. (2000) Transformation of Japanese persimmon (Diospyros kaki Thunb.) with a bacterial gene for choline oxidase. Molecular Breeding 6, 501-510.
28. Gombos Z., Wada H. & Murata N. (1994) The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane lipids: a mechanism of chilling tolerance. Proceedings of the National Academy of Sciences of the United States of America 91, 8787-8791.
29. Gorham J. (1995) Betaines in higher plants - biosynthesis and role in stress metabolism. In Amino Acids and Their Derivatives in Higher Plants (ed. R.M. Wallsgrove) pp. 171-203. Cambridge University Press, Cambridge, UK.
30. Guy C.L. (1990) Cold acclimation and freezing stress tolerance: role of protein synthesis. Annual Review of Plant Physiology and Plant Molecular Biology 41, 187-223.
31. Hakala M., Tuominen I., Keränen M., Tyystjärvi T. & Tyystjärvi E. (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochimica et Biophysica Acta 1706, 68-80.
32. Hall J.L., Harvey D.M.R. & Flowers T.J. (1978) Evidence for the cytoplasmic localization of betaine in leaf cells of Suaeda maritima. Planta 140, 59-62.
33. Hamilton E.W. & Heckathorn S.A. (2001) Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat-shock proteins, whereas complex II is protected by proline and betaine. Plant Physiology 126, 1266-1274.
34. Hanson A.D. & Wyse R. (1982) Biosynthesis, translocation, and accumulation of betaine in sugar beet and its progenitors in relation to salinity. Plant Physiology 70, 1191-1198.
35. Hanson A.D., May A.M., Grumet R., Bode J., Jamieson G.C. & Rhodes D. (1985) Betaine synthesis in chenopods: localization in chloroplasts. Proceedings of the National Academy of Sciences of the United States of America 82, 3678-3682.
36. Hassine A.B., Ghanem M.E., Bouzid S. & Lutts S. (2008) An inland and a coastal population of the Mediterranean xero-halophyte species Atriplex halimus L. differ in their ability to accumulate proline and glycinebetaine in response to salinity and water stress. Journal of Experimental Botany 59, 1315-1326.
37. Hattori T., Mitsuya S., Fujiwara T., Jagendorf A.T. & Takabe T. (2009) Tissue specificity of glycinebetaine synthesis in barley. Plant Science 176, 112-118.
38. Hayashi H., Alia, Mustardy L., Deshnium P., Ida M. & Murata N. (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase: accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. The Plant Journal 12, 133-142.
39. Hayashi H., Alia, Nonaka H., Chen T.H.H. & Murata N. (1998) Enhanced germination under high-salt conditions in seeds of transgenic Arabidopsis expressing a bacterial gene (codA) for choline oxidase. Journal of Plant Research 111, 357-362.
40. Hibino T., Meng Y.L., Kawamitsu Y., et al. (2001) Molecular cloning and functional characterization of two kinds of betaine-aldehyde dehydrogenase in betaine-accumulating mangrove Avicennia marina (Forsk.) Vierh. Plant Molecular Biology 45, 353-363.
41. Hibino T., Waditee R., Araki E., et al. (2002) Functional characterization of choline monooxygenase, an enzyme for betaine synthesis in plants. Journal of Biological Chemistry 277, 41352-41360.
42. Holmstrom K., Somersalo S., Mandal A., Palva T.E. & Welin B. (2000) Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. Journal of Experimental Botany 51, 177-185.
43. Hoque M.A., Banu M.N.A., Okuma E., Amako K., Nakamura Y., Shimoishi Y. & Murata Y. (2007) Exogenous proline and glycinebetaine increase NaCl-induced ascorbate-glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells. Journal of Plant Physiology 164, 1457-1648.
44. Hoque M.A., Banu M.N.A., Nakamura Y., Shimoishi Y. & Murata Y. (2008) Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. Journal of Plant Physiology 165, 813-824.
45. Hsieh T.H., Lee J.T., Yang P.T., Chiu L.H., Charng Y.Y., Wang Y.C. & Chan M.T. (2002a) Heterology expression of the Arabidopsis C-Repeat/Dehydration Response Element Binding Factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiology 129, 1086-1094.
46. Hsieh T.H., Lee J.T., Charng Y.Y. & Chan M.T. (2002b) Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiology 130, 618-626.
47. Huang J., Hirji R., Adam L., Rozwadowski K.L., Hammerlindl J.K., Keller W.A. & Selvaraj G. (2000) Genetic engineering of glycinebetaine production toward enhancing stress tolerance in plants: metabolic limitations. Plant Physiology 122, 747-756.
48. Ishikawa T. & Shigeoka S. (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Bioscience, Biotechnology & Biochemistry 72, 1143-1154.
49. Ito Y., Katsura K., Maruyama K., Taji T., Kobayashi M., Seki M., Shinozaki K. & Yamaguchi-Shinozaki K. (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant & Cell Physiology 47, 141-153.
50. Jagendorf A.T. & Takabe T. (2001) Inducers of glycinebetaine synthesis in barley. Plant Physiology 127, 1827-1835.
51. Kasuga M., Liu Q., Miura S., Yamaguchi-Shinozaki M. & Shinozaki K. (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotechnology 17, 287-291.
52. Kathuria H., Giri J., Nataraja K.N., Murata N., Udayakumar M. & Tyagi A.K. (2009) Glycinebetaine-induced water-stress tolerance in codA-expressing transgenic indica rice is associated with up-regulation of several stress responsive genes. Plant Biotechnology Journal 7, 512-526.
53. Kishitani S., Takanami T., Suzuki M., Oikawa M., Yokoi S., Ishitani M., Alvarez-Nakase A.M., Takabe T. & Takabe T. (2000) Compatibility of glycinebetaine in rice plants: evaluation using transgenic rice plants with a gene for peroxisomal betaine aldehyde dehydrogenase from barley. Plant, Cell & Environment 23, 107-114.
54. Kojima K., Oshita M., Nanjo Y., Kasai K., Tozawa Y., Hayashi H. & Nishiyama Y. (2007) Oxidation of elongation factor G inhibits the synthesis of the D1 protein of photosystem II. Molecular Microbiology 65, 936-947.
55. Kojima K., Motohashi K., Morota T., Oshita M., Hisabori T., Hayashi H. & Nishiyama Y. (2009) Regulation of translation by the redox state of elongation factor G in the cyanobacterium Synechocystis sp. PCC 6803. Journal of Biological Chemistry 284, 18685-18691.
56. Konstantinova T., Parvanova D., Atanassov A. & Djilianov D. (2002) Freezing tolerant tobacco, transformed to accumulate osmoprotectants. Plant Science 163, 157-164.
57. Kumar S., Dhingra A. & Daniell H. (2004) Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confers enhanced salt tolerance. Plant Physiology 136, 2843-2854.
58. Ladyman J.A.R., Hitz W.D. & Hanson A.D. (1980) Translocation and metabolism of glycine betaine in barley plants in relation to water stress. Planta 150, 191-196.
59. Ladyman J.A.R., Ditz K.M., Grumet R. & Hanson A.D. (1983) Genetic variation for glycinebetaine accumulation by cultivated and wild barley in relation to water stress. Crop Science 23, 465-469.
60. Lee J.T., Prasad V., Yang P.T., Wu J.F., Ho D.T.H., Charng Y.Y. & Chan M.T. (2003) Expression of Arabidopsis CBF1 regulated by an ABA/stress-inducible promoter in transgenic tomato confers stress tolerance without affecting yield. Plant, Cell & Environment 26, 1181-1190.
61. Leigh R.A., Ahmad N. & Wyn Jones R.G. (1981) Assessment of glycinebetaine and proline compartmentation by analysis of isolated beet vacuoles. Planta 153, 34-41.
62. Ling M.Y., Wang Y.M., Zhang D.B. & Nii N. (2001) Isolation of a choline monooxygenase cDNA clone from Amaranthus tricolor and its expression under stress conditions. Cell Research 11, 187-193.
63. Lv S., Yang A., Zhang K., Wang L. & Zhang J. (2007) Increase of glycinebetaine synthesis improves drought tolerance in cotton. Molecular Breeding 20, 233-248.
64. McCue K.F. & Hanson A.D. (1990) Drought and salt tolerance: towards understanding and application. Trends in Biotechnology 8, 358-362.
65. McNeil S.D., Rhodes D., Russell B.L., Nuccio M.L., Shachar-Hill Y. & Hanson A.D. (2000) Metabolic modeling identifies key constraints on an engineered glycine betaine synthesis pathway in tobacco. Plant Physiology 124, 153-162.
66. McNeil S.D., Nuccio M.L., Ziemak M.J. & Hanson A.D. (2001) Enhanced synthesis of choline and glycine betaine in transgenic tobacco plants that overexpress phosphoethanolamine N-methyltransferase. Proceedings of the National Academy of Sciences of the United States of America 98, 10001-10005.
67. Mäkelä P., Peltonen-Sainio P., Jokinen K., Pehu E., Setälä H., Hinkkanen R. & Somersalo S. (1996) Uptake and translocation of foliar-applied glycinebetaine in crop plants. Plant Science 121, 221-230.
68. Maritino C.D., Delfine S., Pizzuto R., Loreto F. & Fuggi A. (2003) Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytologist 158, 455-463.
69. Miller G., Suzuki N., Ciftci-Yilmaz S. & Mittler R. (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant, Cell & Environment 33, 453-467.
70. Mohanty A., Kathuria H., Ferjani A., Sakamoto A., Mohanty P., Murata N. & Tyagi A.K. (2002) Transgenics of an elite indica rice variety Pusa Basmati 1 harboring the codA gene are highly tolerant to salt stress. Theoretical and Applied Genetics 106, 51-57.
71. Murata N., Takahashi S., Nishiyama Y. & Allakhverdiev S.I. (2007) Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta 1767, 414-421.
72. Nakamura T., Nomura M., Mori H., Jagendorf A.T., Ueda A. & Takabe T. (2001) An isozyme of betaine aldehyde dehydrogenase in barley. Plant & Cell Physiology 42, 1088-1092.
73. Nishiyama Y., Yamamoto H., Allakhverdiev S.I., Inaba M., Yokota A. & Murata N. (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO Journal 20, 5587-5594.
74. Nishiyama Y., Allakhverdiev S.I., Yamamoto H., Hayashi H. & Murata N. (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43, 11321-11330.
75. Nishiyama Y., Allakhverdiev S.I. & Murata N. (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochimica et Biophysica Acta 1757, 742-749.
76. Nuccio M.L., Russell B.L., Nolte K.D., Rathinasabapathi B., Gage D.A. & Hanson A.D. (1998) The endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. The Plant Journal 16, 487-496.
77. Ohnishi N. & Murata N. (2006) Glycinebetaine counteracts the inhibitory effects of salt stress on the degradation and synthesis of the D1 protein during photoinhibition in Synechococcus sp. PCC 7942. Plant Physiology 141, 756-765.
78. Ohnishi N., Allakhverdiev S.I., Takahashi S., Higashi S., Watanabe M., Nishiyama Y. & Murata N. (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44, 8494-8499.
79. Park E.J. & Chen T.H.H. (2006) Improvement of cold tolerance in horticultural crops by genetic engineering. Journal of Crop Improvement 17, 69-120.
80. Park E.J., Jeknić Z. & Chen T.H.H. (2006) Exogenous application of glycinebetaine increases chilling tolerance in tomato plants. Plant & Cell Physiology 47, 706-714.
81. Park E.J., Jeknić Z., Sakamoto A., DeNoma J., Yuwansiri R., Murata N. & Chen T.H.H. (2004) Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. The Plant Journal 40, 474-487.
82. Park E.J., Jeknić Z., Pino M.T., Murata N. & Chen T.H.H. (2007a) Glycinebetaine accumulation in chloroplasts is more effective than that in cytosol in protecting transgenic tomato plants against abiotic stress. Plant, Cell & Environment 30, 994-1005.
83. Park E.J., Jeknić Z., Chen T.H.H. & Murata N. (2007b) The codA transgene for glycinebetaine synthesis increases the size of flowers and fruits in tomato. Plant Biotechnology Journal 5, 422-430.
84. Peel G.J., Mickelbart M.V. & Rhodes D. (2010) Choline metabolism in glycinebetaine accumulating and non-accumulating near-isogenic lines of Zea mays and Sorghum bicolor. Phytochemistry 71, 404-414.
85. Pino M.T., Skinner J.S., Park E.J., Jeknić Z., Hayes P.M., Thomashow M.F. & Chen T.H.H. (2007) Use of a stress-inducible promoter to drive ectopic AtCBF expression improves potato freezing tolerance while minimizing negative effects on tuber yield. Plant Biotechnology Journal 5, 591-604.
86. Prasad T.K., Anderson M.D., Martin B.A. & Stewart C.R. (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. The Plant Cell 6, 65-74.
87. Prasad K.V.S., Sharmila P., Kumar P.A. & Saradhi P.P. (2000) Transformation of Brassica juncea (L.) Czern. with a bacterial codA gene enhances its tolerance to salt stress. Molecular Breeding 6, 489-499.
88. Quan R., Shang M., Zhang H., Zhao Y. & Zhang J. (2004a) Improved chilling tolerance by transformation with betA gene for the enhancement of glycinebetaine synthesis in maize. Plant Science 166, 141-149.
89. Quan R., Shang M., Zhang H., Zhao Y. & Zhang J. (2004b) Engineering of enhanced glycinebetaine synthesis improves drought tolerance in maize. Plant Biotechnology Journal 2, 477-486.
90. Rajashekar C.B., Zhou H., Marcum K.B. & Prakash O. (1999) Glycine betaine accumulation and induction of cold tolerance in strawberry (Fragaria × ananassa Duch.) plants. Plant Science 148, 175-183.
91. Rathinasabapathi B., Burnet M., Russell B.L., Gage D.A., Liao P.C., Nye G.J., Scott P., Golbeck J.H. & Hanson A.D. (1997) Choline monooxygenase, an unusual iron-sulfur enzyme catalyzing the first step of glycine betaine synthesis in plants: prosthetic group characterization and cDNA cloning. Proceedings of the National Academy of Sciences of the United States of America 94, 3454-3458.
92. Rhodes D. & Hanson A.D. (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annual Review of Plant Physiology & Plant Molecular Biology 44, 357-384.
93. Rhodes D., Rich P.J., Brunk D.G., Ju G.C., Rhodes J.C., Pauly M.H. & Hansen L.A. (1989) Development of two isogenic sweet corn hybrids differing for glycinebetaine content. Plant Physiology 91, 1112-1121.
94. Robinson S.P. & Jones G.P. (1986) Accumulation of glycinebetaine in chloroplasts provides osmotic adjustment during salt stress. Australian Journal of Plant Physiology 13, 659-668.
95. Sakamoto A. & Murata N. (2000) Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance. Journal of Experimental Botany 51, 81-88.
96. Sakamoto A., Alia & Murata N. (1998) Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Molecular Biology 38, 1011-1019.
97. Sakamoto A., Valverde R., Alia, Chen T.H.H. & Murata N. (2000) Transformation of Arabidopsis with the codA gene for choline oxidase enhances freezing tolerance of plants. The Plant Journal 22, 449-453.
98. Schwacke R., Grallath S., Breitkreuz K.E., Stransky E., Stransky H., Frommer W.B. & Rentsch D. (1999) LeProT1, a transporter for proline, glycine betaine, and gamma-amino butyric acid in tomato pollen. The Plant Cell 11, 377-392.
99. Shirasawa K., Takabe T., Takabe T. & Kishitani S. (2006) Accumulation of glycinebetaine in rice plants that overexpress choline monooxygenase from spinach and evaluation of their tolerance to abiotic stress. Annals of Botany 98, 565-571.
100. Smirnoff N. & Cumbes Q.J. (1989) Hydroxyl radical-scavenging activity of compatible solutes. Phytochemistry 28, 1057-1060.
101. Storey R. & Wyn Jones R.G. (1979) Responses of Atriplex spongiosa and Suaeda monoica to salinity. Plant Physiology 63, 156-162.
102. Storey R., Ahmad N. & Wyn Jones R.G. (1977) Taxonomic and ecological aspects of the distribution of glycinebetaine and related compounds in plants. Oecologia 27, 319-332.
103. Su J., Hirji R., Zhang L., He C., Selvaraj G. & Wu R. (2006) Evaluation of the stress-inducible production of choline oxidase in transgenic rice as a strategy for producing the stress-protectant glycinebetaine. Journal of Experimental Botany 57, 1129-1135.
104. Sulpice R., Tsukaya H., Nonaka H., Mustardy L., Chen T.H.H. & Murata N. (2003) Enhanced formation of flowers in salt-stressed Arabidopsis after genetic engineering of the synthesis of glycinebetaine. The Plant Journal 36, 165-176.
105. Takabe T., Hayashi Y., Tanaka A., Takabe T. & Kishitani S. (1998) Evaluation of glycinebetaine accumulation for stress tolerance in transgenic rice plants. In Proceedings of International Workshop on Breeding and Biotechnology for Environmental Stress in Rice pp. 63-68. Hokkaido National Agricultural Experiment Station and Japan International Science and Technology Exchange Center, Sapporo, Japan.
106. Tabuchi T., Kawaguchi Y., Azuma T., Nanmori T. & Yasuda T. (2005) Similar regulation patterns of choline monooxygenase, phosphoethanolamine N-methyltransferase and S-adenosyl-L-methionine synthetase in leaves of the halophyte Atriplex nummularia L. Plant & Cell Physiology 46, 505-513.
107. Takabe T., Rai V. & Hibino T. (2006) Metabolic engineering of glycinebetaine. In Abiotic Stress Tolerance in Plants: Toward the Improvement of Global Environment and Food (eds A. Rai & T. Takabe) pp. 137-151. Springer, Dordrecht, The Netherlands.
108. Takahashi S. & Murata N. (2005) Interruption of the Calvin cycle inhibits the repair of photosystem II from photodamage. Biochimica et Biophysica Acta 1708, 352-361.
109. 2 fixation in the Calvin cycle, is critical for the synthesis of the D1 protein of photosystem II. Biochimica et Biophysica Acta 1757, 198-205.
110. Takahashi S. & Murata N. (2008) How do environmental stresses accelerate photoinhibition? Trends in Plant Science 13, 178-182.
111. Trossat C., Rathinasabapathi B. & Hanson A.D. (1997) Transgenically expressed betaine aldehyde dehydrogenase efficiently catalyzes oxidation of dimethylsulfoniopropionaldehyde and ω-aminoaldehydes. Plant Physiology 113, 1457-1461.
112. Tyystjärvi E. & Aro E.M. (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proceedings of the National Academy of Sciences of the United States of America 93, 2213-2218.
113. Ueda A., Shi W., Sanmiya K., Shono M. & Takabe T. (2001) Functional analysis of salt-inducible proline transporter of barley roots. Plant & Cell Physiology 42, 1282-1289.
114. Valliyodan B. & Nguyen H.T. (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Current Opinions in Plant Biology 9, 1-7.
115. Wada H., Gombos Z. & Murata N. (1994) Contribution of membrane lipids to the ability of the photosynthetic machinery to tolerate temperature stress. Proceedings of the National Academy of Sciences of the United States of America 91, 4273-4277.
116. Waditee R., Bhuiyan M.N.H., Rai V., et al. (2005) Genes for direct methylation of glycine provide high levels of glycinebetaine and abiotic-stress tolerance in Synechococcus and Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 102, 1318-1323.
117. Wang G.P., Li F., Zhang J., Zhao M.R., Hui Z. & Wang W. (2010) Overaccumulation of glycine betaine enhances tolerance of the photosynthetic apparatus to drought and heat stress in wheat. Photosynthetica 48, 30-41.
118. Weigel P., Weretilnyk E.A. & Hanson A.D. (1986) Betaine aldehyde oxidation by spinach chloroplasts. Plant Physiology 82, 753-759.
119. Weretilnyk E.A. & Hanson A.D. (1990) Molecular cloning of a plant betaine-aldehyde dehydrogenase, an enzyme implicated in adaptation to salinity and drought. Proceedings of the National Academy of Sciences of the United States of America 87, 2745-2749.
120. Yamada N., Promden W., Yamane K., Tamagake H., Hibino T., Tanaka Y. & Takabe T. (2009) Preferential accumulation of betaine uncoupled to choline monooxygenase in young leaves of sugar beet - importance of long-distance translocation of betaine under normal and salt-stressed conditions. Journal of Plant Physiology 166, 2058-2070.
121. Yang X., Liang Z. & Lu C. (2005) Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. Plant Physiology 138, 2299-2309.
122. Yang X., Liang Z., Wen X. & Lu C. (2008) Genetic engineering of the biosynthesis of glycinebetaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants. Plant Molecular Biology 66, 73-86.
123. Yang W., Rich P.J., Axtell J.D., Wood K.V., Bonham C.C., Bonham C.C., Ejeta G., Mickelbart M.V. & Rhodes D. (2003) Genotypic variation for glycinebetaine in sorghum. Crop Science 43, 162-169.
124. Yang X., Wen X., Gong H., Lu Q., Yang Z., Tang Y., Liang Z. & Lu C. (2007) Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225, 719-733.
125. Yokota A., Takahara K. & Akashi K. (2006) Water stress. In Physiology and Molecular Biology of Stress Tolerance in Plants (eds K.V.M. Rao, A.S. Raghavendra & K.D. Reddy) pp. 15-39. Springer, Dordrecht, The Netherlands.
126. Zhang J., Tan W., Yang X.H. & Zhang H.X. (2008) Plastid-expressed choline monooxygenase gene improved salt and drought tolerance through accumulation of glycine betaine in tobacco. Plant Cell Reports 27, 1113-1124.
127. Zhao Y., Aspinal D. & Paleg L.G. (1992) Protection of membrane integrity in Medicago sativa L. by glycinebetaine against the effects of freezing. Journal of Plant Physiology 140, 541-543.
128. Zhou S.F., Chen X.Y., Xue X.N., Zhang X.G. & Li Y.X. (2007) Physiological and growth responses of tomato progenies harboring the betaine aldehyde dehydrogenase gene to salt stress. Journal of Integrative Plant Biology 49, 628-637.
129. + antiporter gene SeNHX1. Biotechnology Letters 30, 369-376.